Role of knee ligaments in proprioception and regulation of muscle stiffness

Physiologic evidence for the sensory role of the knee joint ligaments are reviewed. The cruciate and collateral ligaments accomodate morphologically different sensory nerve endings with different capabilities of providing the central nervous system (CNS) with information not only about noxious and chemical stimuli but also about mechanical events, e.g., movement- and position-related stretches of the ligaments. Available data show that low-threshold joint/ligament receptor (i.e., mechanoreceptor) afferents evoke only weak and rare effects in skeletomotor neurons (α-motoneurons), whereas they frequently and powerfully influence fusimotor neurons (γ-motoneurons). The effects on the γ-muscle-spindle system in the muscles around the knee are so potent that even stretches of the cruciate ligaments at relatively moderate loads (not noxious) may induce major changes in responses of the muscle spindle afferents. As the activity in the primary muscle spindle afferents modifies stiffness in the muscles, the cruciate ligament receptors may, through the γ-muscle-spindle system, participate in regulation and preparatory adjustment of the stiffness of the muscles around the knee joint and thereby of knee joint stiffness. Thus, the sensory system of the cruciate ligaments is able to contribute significantly to the functional stability of the knee joint. The possible role of (ligamentous) joint receptors in genesis and spread of muscular tension in occupational muscle pain and in chronic musculoskeletal pain syndromes is also discussed.     

Fusimotor reflex profiles of individual triceps surae primary muscle spindle afferents assessed with multi-afferent recording technique.

The experiments were performed on 21 cats anaesthetized with alpha-chloralose. The aim of the study was to investigate sets of simultaneously recorded spindle afferents (2-4 in each set) from the triceps surae muscle (GS) with respect to the pattern of fusimotor reflex effects evoked by different types of ipsi- and contralateral reflex stimulation. The afferents' responses to sinusoidal stretching of the GS muscle were determined and the fusimotor reflex effects were assessed by comparing the afferent responses (i.e. the mean rate of firing and the depth of modulation) elicited during reflex stimulation with those evoked in absence of any reflex stimulus. Natural of electrical activations of ipsi- and contralateral muscle, skin and joint receptor afferents were used as reflex stimuli. The spindle afferents were influenced by several modalities and from wide areas, with a majority responding to both ipsi- and contralateral stimuli. A particular reflex stimulus often caused different effects on different afferents, and the various reflex stimuli seldom gave similar effects on a particular afferent. Multivariate analysis revealed that the variation in response profiles among simultaneously recorded afferents were as great as between afferents recorded on different occasions. This suggests that the individualized response prifiles, observed in earlier investigations, represent a very diversified reflex control of the spindle primary afferents, and are not a reflection of changes in the setting of the spinal interneuronal network, occurring during the time interval between the recordings of different units. Also, there was no relation between the conduction velocity of the afferents and the reflex profiles of the afferents, but non-linear relations were found between effects elicited by different types of stimuli. Indications were also found that it may be possible to separate the population of GS muscle spindles into subgroups, according to the fusimotor effects exhibited by activation of various categories of ipsi- and contralateral receptor afferents. It is concluded that one possible way of making the very complex reflex system controlling the muscle spindles intelligible may be a combination of multiple simultaneous recordings of spindle afferents and multivariate analysis.     

Fusimotor reflexes influencing secondary muscle spindle afferents from flexor and extensor muscles in the hind limb of the cat.

The purpose of this study was to investigate secondary muscle spindle afferents from the triceps-plantaris (GS) and posterior biceps and semitendinosus (PBSt) muscles with respect to their fusimotor reflex control from different types of peripheral nerves and receptors. The activity of single secondary muscle spindle afferents was recorded from dissected and cut dorsal root filaments in alpha-chloralose anaesthetized cats. Both single spindle afferents and sets of simultaneously recorded units (2-3) were investigated. The modulation and mean rate of firing of the afferent response to sinusoidal stretching of the GS and PBSts muscle were determined. Control measurements were performed in the absence of any reflex stimulation, while test measurements were made during reflex stimulation. The reflex stimuli consisted of manually performed movements of the contralateral hind limb, muscle stretches, ligament tractions and electrical stimulations of cutaneous afferents. Altogether 21 secondary spindle afferents were investigated and 20 different reflex stimuli were employed. The general responsiveness (i.e. number of significant reflex effects/number of control-test series) was 52.4%, but a considerable variation between different stimuli was found, with the highest (89.9%) for contralateral whole limb extension and the lowest (25.0%) for stretch of the contralateral GS muscle. The size of the response to a given stimulus varied considerably between different afferents, and, in the same afferent, different reflex stimuli produced effects of varying size. Most responses were characterized by an increase in mean rate of discharge combined with a decrease in modulation, indicative of static fusimotor drive (Cussons et al., 1977). Since the secondary muscle spindle afferents are part of a positive feedback loop, projecting back to both static and dynamic fusimotor neurones (Appelberg Et al., 1892 a, 1983 b; Appelberg et al., 1986), it is suggested that the activity in the loop may work like an amplified which, during some circumstances, enhance the effect of other reflex inputs to the system (Johansson et al., 1991 b).     

Shoulder reflexes.

Dynamic shoulder stability is dependent on muscular coordination and sensory inputs. In the shoulder, mechanoreceptors are found in the coracoacromial ligament, the rotator cuff tendons, the musculotendinous junctions of the rotator cuff and in the capsule. The number of receptors in the capsule is small compared to the number in the other shoulder structures. Proprioceptive information from numerous receptors in muscles and tendons is mediated via fast conducting nervefibers and probably contribute more to kinaestethic sensation than information from capsule and ligaments. Therefore it seems likely that the joint receptors have a more distinct role for the kinaestethic sense than muscle receptors. In cats a direct reflex from the afferents innervating the shoulder to the muscles around the shoulder has been presented. The reflex had an extremely short latency (2.7-3.1 ms). In man, a very long latency (300 ms) excitatory reflex has been found when nerves in the capsule were stimulated electrically during shoulder surgery. In addition, when the anterior-inferior capsule was excited in conscious humans with modest amplitude electrical stimuli during muscle activity, a strong inhibition was found with an average latency of 33 ms. Stimulation of the sensory nerves in the coracoacromial ligament has also been found to modify muscle activity strongly. Even though our understanding of the control of shoulder motion is incomplete, it is clear that sensory inputs can strongly modify muscle activity around the shoulder. This has implications for rehabilitation and shoulder surgery.     

Different fusimotor reflexes from the ipsi- and contralateral hind limbs of the cat assessed in the same primary muscle spindle afferents

Experiments were performed in forty-five cats anaesthetized with alpha-chloralose. The aim of the study was to investigate a sample of primary muscle spindle afferents from triceps muscle with respect to their fusimotor reflex control from ipsi- as well as contralateral hind limb. Primary muscle spindle afferents of the triceps surae muscle were recorded from the mean rate of firing and the modulation of the afferent response to sinusoidal stretching of the triceps surae muscle was determined. Test measurements were made during tonic stretch of the ipsilateral PBSt, contralateral PBSt, contralateral triceps muscle or during extension of the intact contralateral hind limb. Control measurements were made with ipsi- and contralateral PBSt as well as contralateral triceps muscles relaxed and with contralateral hind limb in resting position. The occurrence and types of fusimotor effects were assessed by comparing test to control responses. The main finding of the present investigation was the great variability in type and size of the fusimotor effects evoked by different ipsi- and contralateral reflex stimuli. Both ipsi- and contralateral stimulations gave rise to predominantly dynamic, predominantly static or mixed static and dynamic fusimotor reflexes. In the same preparation, a given reflex stimulus often caused different reflex responses in different triceps surae primary spindle afferents. In the same afferent unit, different reflex stimuli usually produced fusimotor effects which differed from each other in type and/or size. In general, contralateral whole limb extension and stretch of contralateral PBSt muscles were more potent as reflex stimuli than stretch of the ipsilateral PBSt muscle. Stretch of the contralateral triceps surae muscle was, but for a few afferent units, ineffective as reflexogenic stimulus. It is concluded that the individualized receptive profiles of the primary muscle spindle afferents, which have been postulated in earlier investigations where the effects of different stimuli have been investigated on different cell populations, still seems to hold good when the stimuli are tested on the same units. The individuality of the receptive profiles of gamma-motoneurones is discussed in relation to different motor control hypotheses.     

The effects of cold-induced muscle spindle secondary activity on monosynaptic and stretch reflexes in the decerebrate cat.

The effects of muscle spindle secondary ending activity on the stretch reflex were studied in unanesthetized decerebrate cats. Activation of secondary endings was accomplished by reducing the muscle temperature. This has been shown to cause a sustained asynchronous discharge from secondary endings. Cooling of the medial gastrocnemius or lateral gastrocnemius-soleus muscles caused an increase in the phasic and tonic components of their stretch reflexes. Cooling of the relaxed medial gastrocnemius muscle caused similar increases in the components of the stretch reflex of the synergistic lateral gastrocnemius-soleus muscle and an increase in its monosynaptic reflex. It was concluded that the facilitatory autogenetic and synergistic effects of muscle cooling on the stretch and monosynaptic reflexes were brought about by activity in group II afferents from muscle spindle secondary endings and could not be ascribed to any other type of muscle receptor. These results support the concept of an excitatory role for the secondary endings of the muscle spindle in the stretch reflex of the decerebrate cat.     

Somatosensory activity relevant for motor output. A summary of presentations and discussion

Several aspects of the function of receptors which contribute to somatic sensations are reviewed. First, there is evidence for a role of large-diameter cutaneous afferents in the reflex regulation of precision movements by the hand. Second, large-diameter muscle afferents from the intrinsic muscles of the hand, probably from primary muscle spindle afferents, can evoke specific sensations of finger movement. Third, the variable relationship between discharges in human C fibers from the hand and the specific sensation of pain is investigated. Activity in large-diameter cutaneous afferents can probably modify this sensation. Finally, the properties of small-diameter afferent fibers innervating joints are shown to be consistent with a role in the reflex regulation of joint integrity.     

Neural mechanisms of emesis

Emesis is a reflex, developed to different degrees in different species, that allows an animal to rid itself of ingested toxins or poisons. The reflex can be elicited either by direct neuronal connections from visceral afferent fibers, especially those from the gastrointestinal tract, or from humoral factors. Emesis from humoral factors depends on the integrity of the area postrema; neurons in the area postrema have excitatory receptors for emetic agents. Emesis from gastrointestinal afferents does not depend on the area postrema, but probably the reflex is triggered by projections to some part of the nucleus tractus solitarius. As with a variety of other complex motor functions regulated by the brain stem, it is likely that the sequence of muscle excitation and inhibition is controlled by a central pattern generator located in the nucleus tractus solitarius, and that information from humoral factors via the area postrema and visceral afferents via the vagus nerve converge at this point. This central pattern generator, like those for motor functions such as swallowing, presumably projects to the various motor nuclei, perhaps through interneuronal pathways, to elicit the sequential excitation and inhibition that controls the reflex.     

Relating reflex gain modulation in posture control to underlying neural network properties using a neuromusculoskeletal model

During posture control, reflexive feedback allows humans to efficiently compensate for unpredictable mechanical disturbances. Although reflexes are involuntary, humans can adapt their reflexive settings to the characteristics of the disturbances. Reflex modulation is commonly studied by determining reflex gains: a set of parameters that quantify the contributions of Ia, Ib and II afferents to mechanical joint behavior. Many mechanisms, like presynaptic inhibition and fusimotor drive, can account for reflex gain modulations. The goal of this study was to investigate the effects of underlying neural and sensory mechanisms on mechanical joint behavior. A neuromusculoskeletal model was built, in which a pair of muscles actuated a limb, while being controlled by a model of 2,298 spiking neurons in six pairs of spinal populations. Identical to experiments, the endpoint of the limb was disturbed with force perturbations. System identification was used to quantify the control behavior with reflex gains. A sensitivity analysis was then performed on the neuromusculoskeletal model, determining the influence of the neural, sensory and synaptic parameters on the joint dynamics. The results showed that the lumped reflex gains positively correlate to their most direct neural substrates: the velocity gain with Ia afferent velocity feedback, the positional gain with muscle stretch over II afferents and the force feedback gain with Ib afferent feedback. However, position feedback and force feedback gains show strong interactions with other neural and sensory properties. These results give important insights in the effects of neural properties on joint dynamics and in the identifiability of reflex gains in experiments.     

Sensorimotor pathways involved in interjoint reflex action of an insect leg

Coordination of motor output between leg joints is crucial for the generation of posture and active movements in multijointed appendages of legged organisms. We investigated in the stick insect the information flow between the middle leg femoral chordotonal organ (fCO), which measures position and movement in the femur-tibia (FT) joint and the motoneuron pools supplying the next proximal leg joint, the coxa-trochanteral (CT) joint. In the inactive animal, elongation of the fCO (by flexing the FT joint) induced a depolarization in eight of nine levator trochanteris motoneurons, with a suprathreshold activation of one to three motoneurons. Motoneurons of the depressor trochanteris muscle were inhibited by fCO elongation. Relaxation signals, i.e., extension of the FT joint, activated both levator and depressor motoneurons; i.e., both antagonistic muscles were coactivated. Monosynaptic as well as polysynaptic pathways contribute to interjoint reflex actions in the stick insect leg. fCO afferents were found to induce short latency EPSPs in levator motoneurons, providing evidence for direct connections between fCO afferents and levator motoneurons. In addition, neuronal pathways via intercalated interneurons were identified that transmit sensory information from the fCO onto levator and/or depressor motoneurons. Finally, we describe two kinds of alterations in interjoint reflex action: (a) With repetitive sensory stimulation, this interjoint reflex action shows a habituation-like decrease in strength. (b) In the actively moving animal, interjoint reflex action in response to fCO elongation, mimicking joint flexion, qualitatively remained the same sign, but with a marked increase in strength, indicating an increased influence of sensory signals from the FT joint onto the adjacent CT joint in the active animal. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 891–913, 1997     

Somatosensory unit input to the spinal cord during normal walking

Chronic recording techniques in freely walking cats have been used to sample unitary activity from most large myelinated afferent classes. Cutaneous mechanoreceptors are highly sensitive and generate regular activity patterns predictable from their modalities. Knee joint afferents can fire briskly midrange locomotory movements but appear to be influenced by factors other than joint angle. Golgi tendon organs generate activity consistent with sensitivity to active muscle tension. Muscle spindle afferents do not appear to conform to any single functional pattern for all muscles. It is suggested that degree and rate of stretch are sensed by spindles (possibly under dynamic fusimotor bias) in extensor muscles which normally undergo isometric or lengthening contractions whereas rapidly modulated static fusimotor activity is employed to preserve spindle activity during the rapidly shortening contractions of flexor muscles. Both patterns may be represented in different spindles of bifunctional, biarticular muscles such as rectus femoris and sartorius.     

Analyses of dynamic co-contraction level in individuals with anterior cruciate ligament injury.

BACKGROUND: A complete understanding of neural mechanisms by which ligament receptors may contribute to joint stability is not well established. It has been suggested that these receptors may be involved in a neuromuscular process related to the modulation of dynamic co-contraction, as a means of guaranteeing functional joint stability. HYPOTHESIS: Individuals with ACL injury have diminished dynamic co-contraction. STUDY DESIGN: Exploratory, cross-sectional design. METHODS: Ten subjects with unilateral ACL injury treated conservatively, and ten subjects without history of injury participated in the study. The co-contraction level was assessed through EMG recordings of the vastus lateralis and biceps femoris before and after a perturbation imposed on the subjects during a walking task. RESULTS: Subjects with ACL injury presented significantly lower co-contraction level pre-perturbation (p = 0.045) and post-perturbation (p = 0.046) than those in the control group. CONCLUSIONS: The bilateral decrease in muscular co-contraction presented by individuals with ACL injury suggests that ligament and joint receptors may be responsible for a bilateral dynamic increase in muscle and joint stiffness that could result in a greater joint stability. CLINICAL RELEVANCE: This study analyzed a neuromuscular mechanism that might contribute to the functional stability of the knee joint.     

Separation and estimation of muscle spindle and tension receptor populations by vibration of the biceps muscle in the frog

Frog spinal cord reflex behaviors have been used to test the idea of spinal primitives. We have suggested a significant role for proprioception in regulation of primitives. However the in vivo behavior of spindle and golgi tendon receptors in frogs in response to vibration are not well described and the proportions of these proprioceptors are not established. In this study, we examine the selectivity of muscle vibration in the spinal frog. The aim of the study was (1) to examine how hindlimb muscle spindles and GTO receptors are activated by muscle vibration and (2) to estimate the relative numbers of GTO receptors and spindle afferents in a selected muscle, for comparison with the mammal. Single muscle afferents from the biceps muscle were identified in the dorsal roots. These were tested in response to biceps vibration, intramuscular stimulation and biceps nerve stimulation. Biceps units were categorized into two types: First, spindle afferents which had a high conduction velocity (approximately 20-30 m/s), responded reliably (were entrained 1:1) to muscle vibration, and exhibited distinct pauses to shortening muscle contractions. Second, golgi tendon organ afferents, which had a lower conduction velocity (approximately 10-20 m/s), responded less reliably to muscle vibration at physiologic muscle lengths, but responded more reliably at extended lengths or with background muscle contraction, and exhibited distinct bursts to shortening muscle contractions. Vibration responses of these units were tested with and without muscle curarization. Ensemble (suction electrode) recordings from the dorsal roots were used to provide rough estimates of the proportions of the two muscle afferent types.     

The effects of acute and prolonged muscle vibration on the function of the muscle spindle’s reflex arc

Abstract

Purpose:?Localized mechanical vibration, applied directly to a muscle, is known to have powerful, duration-dependent effects on the muscle spindle’s reflex arc. Here, the conditioning of the function of the spindle reflex arc via vibration was examined with considerations for use as a non-invasive, sensorimotor research tool.

Methods:?Muscle spindle function was examined with patellar tendon taps prior to and following exposure to muscle vibration applied to the quadriceps femoris for acute (<5?s) and prolonged (20?min) durations. Surface electromyography (sEMG), torque, and accelerometry signals were obtained during the taps to quantify various measures of reflex magnitude and latency.

Results:?Our findings suggest that acute vibration had no effect on normalized reflex torque or sEMG amplitude (p?>?0.05), but increased total reflex latency (p?=?0.022). Alternatively, prolonged vibration reduced normalized reflex torque and sEMG amplitude (p?<?0.001), and increased reflex latency (p?<?0.001).

Conclusions:?Our findings support the use of prolonged vibration as a practical means to decrease the function of the muscle spindle’s reflex arc. Overall, this suppressive effect was evident in the majority of subjects, but the extent was variable. This approach could potentially be used to help delineate the muscle spindle’s role in various sensory or motor tasks in which more direct measures are not feasible. Acute vibration, however, did not potentiate muscle spindle function as hypothesized. Rather, our results suggest that acute vibration increased total reflex latency. Accordingly, potential mechanical and neurophysiological mechanisms are discussed.     

Direct and relayed projection of periodontal receptor afferents to the cerebellum in the ferret

Field potentials in the cerebellar cortex of the ferret have been studied in response to stimulation of alveolar, muscular and cutaneous branches of the trigeminal nerve. Responses from the alveolar nerves are unusual in their very short latency. Evidence based on latency analysis, frequency following and comparison with other well-known inputs supports the view that the earliest field potentials are due to direct, unrelayed afferents, which terminate as mossy fibres. There is, in addition, a monosynaptically relayed afferent path via mossy fibres. The alveolar nerve afferents concerned with the direct projection are shown to come from periodontal mechanoreceptors and not from cutaneous receptors. No such connections are found from jaw-muscle spindle afferents. The direct and relayed periodontal pathways are both ipsilateral and crossed. They terminate in the cerebellar cortex in the parvermal region of lobules IV, V and VI. The functional significance of the direct periodontal afferent projection is considered particularly in the light of parallels with the vestibular system, which also has direct and relayed cerebellar projections.     

Modulation of human muscle spindle discharge by arterial pulsations--functional effects and consequences

Arterial pulsations are known to modulate muscle spindle firing; however, the physiological significance of such synchronised modulation has not been investigated. Unitary recordings were made from 75 human muscle spindle afferents innervating the pretibial muscles. The modulation of muscle spindle discharge by arterial pulsations was evaluated by R-wave triggered averaging and power spectral analysis. We describe various effects arterial pulsations may have on muscle spindle afferent discharge. Afferents could be "driven" by arterial pulsations, e.g., showing no other spontaneous activity than spikes generated with cardiac rhythmicity. Among afferents showing ongoing discharge that was not primarily related to cardiac rhythmicity we illustrate several mechanisms by which individual spikes may become phase-locked. However, in the majority of afferents the discharge rate was modulated by the pulse wave without spikes being phase locked. Then we assessed whether these influences changed in two physiological conditions in which a sustained increase in muscle sympathetic nerve activity was observed without activation of fusimotor neurones: a maximal inspiratory breath-hold, which causes a fall in systolic pressure, and acute muscle pain, which causes an increase in systolic pressure. The majority of primary muscle spindle afferents displayed pulse-wave modulation, but neither apnoea nor pain had any significant effect on the strength of this modulation, suggesting that the physiological noise injected by the arterial pulsations is robust and relatively insensitive to fluctuations in blood pressure. Within the afferent population there was a similar number of muscle spindles that were inhibited and that were excited by the arterial pulse wave, indicating that after signal integration at the population level, arterial pulsations of opposite polarity would cancel each other out. We speculate that with close-to-threshold stimuli the arterial pulsations may serve as an endogenous noise source that may synchronise the sporadic discharge within the afferent population and thus facilitate the detection of weak stimuli.     

Activation of human arm muscles during flexion/extension and supination/pronation tasks: A theory on muscle coordination

Generally the number of muscles acting across a joint exceeds the number of degrees of freedom available to the joint. This redundancy raises a problem regarding the ratio in which these muscles are activated during a particular motor task. In this paper we present a theory to explain the activation patterns of muscles used during voluntary and reflex induced contractions. The basic assumptions underlying the theory are that 1) coordination of muscles is based on synergistic muscle activities, 2) the synergisms involved satisfy certain transformations of muscle spindle signals to muscle activation signals and 3) muscle spindle output is proportional to the ratio of muscle stretch and muscle length in lengthening muscles, and is zero in shortening muscles. The theory is used to predict the recruitment threshold of motor units in six arm muscles during voluntary isometric contractions. All theoretical predictions are in reasonable agreement with the experimentally observed behavior of a large population of motor units within each muscle. However, within a single muscle sometimes motor-unit populations have been found to have different types of recruitment behavior. This deviating behavior is discussed in the light of the theory presented here.     

Probing the neuromodulatory gain control system in sports and exercise sciences

The monoaminergic bulbospinal pathways from the brainstem are central to motor functions by regulating the gains of spinal motoneurons and represent, in that respect, probably the primary control system for motoneuron excitability. Yet, the efficiency of this system is few, if not never, assessed in the fields of sports and exercise sciences. In this review paper, we propose a methodological approach intended to assess how this neuromodulatory system affects motoneuron excitability. This approach is based on the use of tendon vibration which can, in certain circumstances, induce the generation of the so-called tonic vibration reflex through the stimulation of muscle spindles. Force and EMG responses to tendon vibration are indeed indicative of how this descending system modulates the gain of the ionotropic inputs from Ia afferents and thus of the strength of the monoaminergic drive. After a brief presentation of the neuromodulatory system and of the mechanisms involved in the generation of the tonic vibration reflex, we address some important methodological considerations regarding the use of the TVR to probe this neuromodulatory gain control system. Hopefully, this paper will encourage sports and exercise scientists to investigate this system.     

Functional coordination of motor activity in colonic smooth muscles in rat experimental model

Spontaneous and electrically-elicited motor activity was recorded by triple organ bath in rat segment-model preparation as display of excitation of local nerve networks and ascending or descending reflex pathways underlying contractile potency and functional coordination of colonic longitudinal and circular muscles. Spontaneous high-amplitude contractions, but not relaxations, appeared synchronously in both muscles. Electrical field stimulation applied to proximal or distal part of segments elicited both tetrodotoxin (0.1 microM)-sensitive local motor responses of the stimulated part and ascending or descending motor responses of the contralateral, nonstimulated part of the preparations. Contractions characterized the local response of longitudinal muscle. The circular muscle responded with relaxation followed by contraction. Synchronous ascending contractions and descending contraction of the longitudinal muscle and relaxation followed by contraction of the circular muscle were observed when the middle part of segments was stimulated, thus indicating that locally-induced nerve excitation propagated via intrinsic ascending or descending nerve pathways that could be synchronously coactivated by one and the same stimulus. The ascending motor responses were more pronounced and the motor responses of longitudinal muscle were expressed more than those of circular muscle suggesting an essential role of ascending reflex pathways and longitudinal muscle in the coordinated motor activity of colon.